Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 118, Issue 22, Pages -Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.2017890118
Keywords
specialized metabolism; stress response; glucosinolate; sulfur
Categories
Funding
- Japan Society for the Promotion of Science (JSPS) KAKENHI [16H07449, 18K14348, 19H02859, 20H04852]
- RIKEN Special Postdoctoral Researcher Program
- China Scholarship Council [201906610013]
- Grants-in-Aid for Scientific Research [20H04852, 19H02859, 18K14348, 16H07449] Funding Source: KAKEN
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The study demonstrates that sulfur-rich plant metabolites, glucosinolates, can be reintegrated into primary metabolism in Arabidopsis thaliana, serving as a sulfur source to recover invested resources. It reveals the catabolic processing of glucosinolate breakdown products, mobilizing sulfur from the thioglucoside group, and the role of specific enzymes in this process. Overall, the findings highlight the bidirectional interaction between primary and specialized metabolism in plants.
Specialized (secondary) metabolic pathways in plants have long been considered one-way routes of leading primary metabolite precursors to bioactive end products. Conversely, endogenous degradation of such end products in plant tissues has been observed following environmental stimuli, including nutrition stress. Therefore, it is of general interest whether specialized metabolites can be reintegrated into primary metabolism to recover the invested resources, especially in the case of nitrogen- or sulfur-rich compounds. Here, we demonstrate that endogenous glucosinolates (GLs), a class of sulfur-rich plant metabolites, are exploited as a sulfur source by the reallocation of sulfur atoms to primary metabolites such as cysteine in Arabidopsis thaliana. Tracer experiments using 34S- or deuterium-labeled GLs depicted the catabolic processing of GL breakdown products in which sulfur is mobilized from the thioglucoside group in GL molecules, potentially accompanied by the release of the sulfate group. Moreover, we reveal that beta-glucosidases BGLU28 and BGLU30 are the major myrosinases that initiate sulfur reallocation by hydrolyzing particular GL species, conferring sulfur deficiency tolerance in A. thaliana, especially during early development. The results delineate the physiological function of GL as a sulfur reservoir, in addition to their well-known functions as defense chemicals. Overall, our findings demonstrate the bidirectional interaction between primary and specialized metabolism, which enhances our understanding of the underlying metabolic mechanisms via which plants adapt to their environments.
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